Received: 1 December 2017 | Revised: 19 January 2018 | Accepted: 19 January 2018 DOI: 10.1002/ajpa.23429 CENTENNIAL PERSPECTIVE 100 years of primate paleontology Richard F. Kay Department of Evolutionary Anthropology and Division of Earth and Ocean Sciences, Duke University, Durham, North Carolina 27708 Correspondence Richard F. Kay, Duke University, Box 90383, Department of Evolutionary Anthropology, Durham, NC 27708. Email: [email protected] KEYWORDS: biogeography, euprimate origins, Haplorhini, paleobiology, Plesiadapiformes, Primates, Strepsirrhini and Malaysia is one of the most urgent scientific neces- sities (Hrdlička, 1918). From the first growth of the tree, many a limb and branch has decayed and dropped off; and these lost Members of the Association continue to recognize the need to branches of various sizes may represent those whole document human ancestry and its roots. The mission statement of the orders, families, and genera which have now no living Association states: “Physical anthropology is a biological science that representatives, and which are known to us only from deals with the adaptations, variability, and evolution of human beings having been found in a fossil state.... As buds give rise and their living and fossil relatives.” This begs the question as to how by growth to fresh buds, and these, if vigorous, branch closely related to humans a primate needs to be for it to fall within the out and overtop on all sides many a feebler branch, so confines of physical anthropology. A narrow reading of the Associa- by generation I believe it has been with the great Tree tion’s mission could imply, for example, that the evolution of lemurs of Life, which fills with its dead and broken branches and lorises and their extinct relatives might well be outside the Associa- the crust of the earth, and covers the surface with its tion’s mission. Fortunately, that has not been the case, as demonstrated ever branching and beautiful ramifications. (p 129,130 in meeting abstracts and publications in the Journal. Moreover, the in Darwin 1859). National Science Foundation, a primary source for paleoprimatology research funding, mentions nonhuman primate paleontology as an area it supports. 1 | PRIMATE PALEONTOLOGY AS A Up until the 1960s, most of the work of primate paleontology was DISCIPLINE WITHIN BIOLOGICAL focused upon humans and their ancestors. Many studies of Miocene ANTHROPOLOGY and earlier primates were undertaken by comparative anatomists and broadly-trained vertebrate paleontologists. Fossil primate studies were In 1918, Ales Hrdlička, Curator, Division of Physical Anthropology, largely carried out by paleontologists interested in paleofaunas that U. S. National Museum and founder of the American Association of contained primates, for example, the works of C. L. Gazin, J. W. Gidley, Physical Anthropology and this journal, recognized paleoprimatology as W. Granger, W. D. Matthew, M. Schlosser, G. G. Simpson, H. G. Stehlin, a distinct branch of physical anthropology, albeit with the assumption or F. Ameghino. Or fossils were incorporated into broader works by that fossil primates might tell us about human origins: those with a primary research interest in human and comparative anat- omy, for example by Wilfrid Le Gros Clark (1934, 1959). The remains of the fossil forms of the primates are William K. Gregory was a notable exception. While he maintained unfortunately still few in number and very defective; a broad research scope including study of Recent and fossil fishes, rep- nevertheless, they are being gradually augmented, and tiles, and mammals other than primates, he made seminal contributions the hope seems justified that in the not far distant to primate paleontology. In 1916, he published a study of the early future forms will be recovered that will be of as acute stages of anthropoid evolution (Gregory, 1916). This work was fol- interest to the student of man’s origin as the known lowed by a landmark study of the anatomy of a well-preserved skele- remains of some of his earlier representatives. An inten- ton of the North American Eocene ‘lemur’ Notharctus (Gregory, 1920). sive systematic search for such remains in Africa, Asia, Gregory’s synthetic work on the evolution of the human dentition 652 | VC 2018 Wiley Periodicals, Inc. wileyonlinelibrary.com/journal/ajpa Am J Phys Anthropol. 2018;165:652–676. KAY | 653 (1922) influenced every primate paleontologist going forward. It brought his broad expertise on the anatomy of living primates to bear on the early fossil record of primates. Notably also, he called to the attention of the North American paleontological community the work of European paleontologists and comparative anatomists. Paleoprimatology as a discipline really took off in the early 1960s with the establishment of primate-centered fossil studies at Yale Uni- versity under the direction of Elwyn Simons (1930–2016). Having received his early training in vertebrate paleontology at Princeton University studying a group of Paleocene-Eocene ungulates, Simons FIGURE 1 Date of description of fossil primates (including Euprimates and Plesiadapiformes) since the first description of a moved on to Oxford University, working with Le Gros Clark. At first, primate fossil (Adapis Cuvier 1821). 13% of taxa recognized today Simons was best known for his revival of GE Lewis’ (1934) claims for were known at the time of the founding of the American Journal of Ramapithecus as a mid-Miocene human ancestor. However, Simons’s Physical Anthropology work under Le Gros Clark on Paleocene and Eocene primates from Europe also rekindled interest in Paleogene primates. In this way, and (https://en.wikipedia.org/wiki/List_of_fossil_primates). Just 43, or 13%, through Simons’ efforts, there was a broadening of paleoanthropol- of these taxa had been described by the time of the founding of the ogy to include the whole primate record. Like Gregory, Simons American Journal of Physical Anthropology in 1918 (Figure 1). In spite of emphasized the importance of understanding human evolution within the vastly improved record since then, primate fossils remain woefully the framework of the evolution of primates and their relatives in the scarce. Consider that there are 79 genera of living primates (18 in Asia; whole of the Cenozoic. Always dismissive of “armchair” paleontolo- 24 in Africa; 15 in Madagascar; 19 in South America; 4 in Central gists who primarily were interested in studying fossils that had America) [including some overlaps] and more than 504 species (Estrada already been collected, Simons placed an enormous emphasis on et al., 2017). Hypothetically, if the average primate genus persists 3 mil- gathering new fossils. He and his students returned to fossil fields lion years, then a minimum of 1300 genera and 10,000 species may that had lain fallow for half a century or more in India, Pakistan, and > have existed over the 65 million years of primate evolution. But even Egypt. He undertook broad collaborative field programs to recover fossil primates from Madagascar and the Western United States. the 336 known fossil genera are mostly based on scant remains, mainly Simons trained and worked with several generations of Yale, and jaws and teeth, which in turn constrains our ability to test scenarios of later Duke University students who embodied his notion of the cen- primate evolution. Before 1918 the record of fossil primates was mainly from North tral importance of assembling new fossil collections. Although similar America and Europe, outside the current tropical distribution of non- programs were developing in parallel in Great Britain under the influ- human primates. Just two genera were described from South America, ence of John Napier and P. R. Davis and at a few other US institu- tions, for example at the American Museum of Natural History by one from Asia, four from continental Africa, and six from the the students of Malcolm McKenna (Fred Szalay, Eric Delson, and Pleistocene-Recent of Madagascar. More regions of the globe are now their students), Simons may fairly be described as the father of mod- sampled to some extent but critical gaps remain. For example, primates ern paleoprimatology. inhabited Africa since the Early Paleogene; but of 82 extinct genera In what follows, I present a highly personal account of trends and thus far described, just five are more than 40 million years old and the threads that comprise paleoprimatology, emphasizing how develop- record of subtropical and southern parts of the continent is virtually nil. ments in other fields that greatly influenced the way we think about And, although primates must have resided in Madagascar since the fossil primates in time, in space, and in relation to the environments in Eocene, the primate fossil record is entirely from the Pleistocene-to- which they lived. I evaluate the evidence for one of the most contested Recent. In South America (including Central America and the Greater aspects of primate evolution. How and when did primate adaptations Antilles), just 26 extinct genera are recorded, which is barely more than evolve? the generic count of living taxa. Platyrrhines as old as 40 million years should be expected but none is older than 30 million years, and virtu- 2 | THE PLACE OF PRIMATES AMONG ally no tropical or subtropical sites are known prior to 15 million years MAMMALS AND THE SHAPE OF THE ago. PRIMATE TREE 2.2 | Where do primates fit in the mammalian tree? 2.1 | The rich but incomplete primate fossil record When I began my graduate studies at Yale University with Elwyn The fossil record of primates has grown enormously in the past Simons almost half a century ago, William K. Gregory’s (1910) and 100 years but primate species are still relatively rare (Martin 1993). As George G. Simpson’s (1945) influential works on the relations of prima- of 2017, 336 extinct genera of primates were recognized on the Paleo- tes to other mammals were canonical.